Adaptations in the role of pharmacists under the conditions of the COVID-19 pandemic: a systematic review and meta-analysis

Background Community pharmacists actively engage in managing the health of local residents, but the COVID-19 pandemic has necessitated rapid adaptations in practice activities. Objectives We sought to identify the specific adaptations in practice and the expanded roles of community pharmacists in response to the COVID-19 pandemic. Methods We conducted a systematic review of published studies reporting the tasks of pharmacists in community pharmacies or who were involved in pharmacy practices addressing the pandemic. Two investigators independently searched PubMed (December 2019–January 2022) for eligible articles. We conducted a meta-analysis to measure the frequencies of practical activities by pharmacists in response to COVID-19. Results We identified 30 eligible studies. Meta-analysis of these studies found that the most commonly reported adaptation in pharmacist practice activities was modifying hygiene behaviors, including regular cleaning and disinfection (81.89%), followed by maintaining social distance from staff and clients (76.37%). Educating clients on COVID-19 was reported by 22 studies (72.54%). Telemedicine and home delivery services were provided to clients by 49.03 and 41.98% of pharmacists, respectively. Conclusions The roles of community pharmacists in public health activities have adapted and expanded in response to COVID-19, notably by incorporating public health education activities. Supplementary Information The online version contains supplementary material available at 10.1186/s12913-023-09071-w.

Understanding the adaptations in pharmacists' practice during the COVID-19 pandemic is crucial to strengthening the role of pharmacists as health partners to the community and for developing effective countermeasures to COVID-19 and potential future infectious disease pandemics. Previous reviews have mentioned the potential for community pharmacists to play an important role in the COVID-19 pandemic by taking on a variety of new roles that complement their existing work [20][21][22]. However, no comprehensive, systematic review and metaanalysis focusing on pharmacists' practice during the era of the COVID-19 pandemic has been conducted.
The purpose of the present study is to examine the adaptations to the practice of community pharmacists in response to COVID-19 conditions, and how these adaptations contributed to public health and infection preventions, in an effort to provide an evidence base for discussing the role of pharmacists in future pandemics due to emerging infectious diseases.

Methods
This systematic review and meta-analysis was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement and the statement by the Meta-analysis of Observational Studies in Epidemiology (MOOSE) group [23,24] (see Additional file 1).

Eligibility criteria and outcome measures
Studies from the PubMed database fulfilling the following selection criteria were included in the meta-analysis: (1) randomized clinical trials, observational studies, letters and commentaries in the IMRD (introduction, methods, results, discussion) format written in the English language; (2) with a study population of pharmacists or others involved in pharmacy practices regarding COVID-19; (3) with primary outcomes of practical activities performed by pharmacists for COVID-19; (4) with outcome variables of pharmacy practices regarding COVID-19 in categories of drug and information delivery, client education, regular cleaning and disinfecting, and structural ingenuity; and (5) with any secondary outcome variable.
The exclusion criteria were as follows: (1) studies of practical activities such as equipment and disinfection to protect individual pharmacists; (2) studies without reporting of outcome variables; and (3) studies with insufficient or incomplete data. We selected all reported outcome variables from the extracted papers and selected same reported variables in these reports as the outcome variables in the present study.
The main focus of this review was community pharmacists. However, it is necessary to understand what happened in hospitals to fully understand the situation relating to community pharmacists.

Information sources and search strategy
Two investigators (D.K. and T.M.) independently searched for eligible studies published in PubMed, and the Cochrane Library from 1 December 2019 to 31 January 2022. We used the following key words: "novel coronavirus" OR "new coronavirus" OR "emerging coronavirus" OR "2019-nCoV" OR "COVID-19" OR "SARS-CoV-2" AND "pharmacist" OR "chemist" OR "apothecary" OR "pharmaceutist" OR "druggist". We also reviewed the reference lists of eligible studies using Google Scholar and performed a manual search to ensure that all appropriate studies were included.

Data extraction
Two investigators (D.K. and T.M.) independently searched for eligible studies. Articles obtained from the search were stored in Citation Manager (EndNote 20; Thomson Reuters, New York, NY, USA). After removing redundant articles, we examined the titles, abstracts, and full-text articles. Then, we extracted the data for country, methodology, study design, study participants, study site, sample size, study period, and main focus of each study. Outcome variables were extracted into pre-designed data collection forms. Data accuracy was verified by comparing the collection forms of each investigator, any discrepancies were determined through discussion [25].

Level of evidence
The level of evidence was determined based on the Grading of Recommendations, Assessment, Development, and Evaluations (GRADE) framework, which classifies the level of evidence for each outcome based on the risk of bias, imprecision, inconsistency, indirectness, and publication bias [26]. The authors classified the evidence level for each eligible study according to the revised grading system for recommendation in the evidence base guideline (see Additional file 2) [27].

Data analysis
Throughout the meta-analysis, we calculated the prevalence of each outcome variable with 95% confidence intervals (CIs) using a random-effects model (generic inverse variance method). To assess the prevalence of the outcome variables among pharmacy practices, the standard error was calculated using the Agresti-Coull method [28]. Heterogeneity among the original studies was evaluated using the I 2 statistic [29]. Publication bias was examined using a funnel plot. For all analyses, significance levels were two-tailed, and p < 0.05 was considered significant. All statistical tests were performed using Review Manager (RevMan) Version 5.4.1 (Cochrane Collaboration, Copenhagen, Denmark) [30].

Study selection and characteristics
The initial database search identified 497 candidate publications. Of these, 30 studies [3-13, 15-19, 31-44] reported the outcome variables that met eligibility criteria (Fig. 1). Table 1 shows the characteristics of the included studies.
Of the 30 studies, 27 were cross-sectional studies [3-13, 15, 17, 18, 31-33, 35-44] and 3 were retrospective observational studies based on electronic health records [16,19,34]. Although most survey participants in the cross-sectional studies were pharmacists, several studies included customers or patients using community pharmacies [17,43], home treatment patients [42], and community residents [5] whose responses also indicated pharmacy practices regarding COVID-19. In this study, the largest number of studies on pharmacists' practices regarding COVID-19 came from the West Asian region with 9 studies [7,11,17,32,[39][40][41][42]44], the most common country of origin for studies was Jordan [17,32,39,40]. Table 2 presents the major outcomes of studies of pharmacist practices regarding COVID-19.   Various public health activities were commonly carried out, although the activities reported by pharmacists differed. These outcome variables were integrated into similar categories to estimate the percentage of pharmacist practice activities.

Evaluation of pharmacy practice activities for COVID-19
Thirty studies had data on any of the items that met the eligibility criteria [3-13, 15-19, 31-44]. Among the 30 studies with data on the primary outcome, we used metaanalysis to estimate the proportion of pharmacy operations related to COVID-19 in the categories of drugs and information delivery, client education, cleaning and disinfecting regularly, and structural ingenuity for each item.
The estimated proportion of pharmacists who provided telemedicine and home delivery services, classified as drugs and information delivery, were 49.03 and 41.98% respectively (Fig. 2); those who reported providing education for clients regarding COVID-19 was 72.54% (Fig. 3). In the hygiene behaviors item, the estimated proportions of pharmacists who cleaned and disinfected regularly and kept social distance with staff and clients was 81.89 and 76.37%, respectively (Fig. 4). In the structural ingenuity item, 63.88 and 51.00% of the respondents implemented restricted entrance to the pharmacy and restricted access area in the pharmacy, respectively (Fig. 5). Table 2 presents the various outcomes reported in each study. Of the 30 studies showing pharmacy practice for COVID-19, most focused on community pharmacists; four studies reported on only hospital and clinical pharmacists [15,16,19,34].

Secondary outcomes
Pharmacy practices other than the primary outcome included one report in which "clinical pharmacists recommended medication" for COVID-19 patients admitted to the ICU [34], as well as a report in which community pharmacists limited the number of items per client purchase to eliminate shortages of dietary supplements and medications [37].

Discussion
The present study quantified the extent to which pharmacists are engaged in various public health activities for COVID-19 that augment health and infection prevention strategies for local residents. The most common practice activity of pharmacists in the response to COVID-19 was providing education for community residents.
COVID-19 is an emerging infectious disease with various factors, including prevention and treatment, that are evolving or were unknown, especially in the early days of the pandemic. People needed reliable information relating to COVID-19 and sought out healthcare professionals to provide them the appropriate and necessary information. In fact, in our previous study conducted in the first phases of the pandemic, community pharmacists received more questions from clients regarding COVID-19 than questions regarding drugs and medications [3].
Pharmacists are trusted community health care providers and are not only required to provide consultations as drug experts, but also to provide the necessary information to community residents in an easy-to-understand manner [45]. A scoping review of the role of pharmacists during the COVID-19 pandemic likewise reported that the pharmacist's primary role was to provide information and counseling to patients [20]. Especially in an emergency situation in the setting of an emerging infectious disease pandemic, pharmacists must adjust their role to place greater emphasis on providing necessary information, conducting consultations and educating local residents. In addition, to augment the information publicly accessible via the media or the internet [3,9,36,39], pharmacists have greater access to reliable scientific information from international organizations such as the World Health Organization and scientific and medical evidence than do the public they serve [4,11,32,35,41]. This education is the most effective and crucial way to provide information to local residents. In fact, the educational programs conducted by pharmacists for older adults can focus on both the drug regimens for management of their chronic diseases as well as simultaneously on precautions for the personal hygiene management and the necessity of securing physical distance to assist in the prevention of COVID-19 [5,7,8,10,12,32,41]. Some pharmacists' practice activities adapted to include creating brochures and effectively using visual posters to educate clients about COVID-19 [8,33,35]. The results of the present study showing the high frequency of pharmacists providing education to local residents may result from their high level of understanding and motivation of this aspect as a major part of their professional role.
To impede the spread of the COVID-19 epidemic and to curb the impact of many unreliable or intentionally misleading news stories, community pharmacies in Italy worked with the Italian Ministry of Health and others to provide information to the local population on public health responses [13]. This "fake news" not only spreads inaccurate knowledge but has also been reported to have negative health effects on people, including various psychological disorders and fatigue [46]. In many countries, the role of pharmacists has shifted from targeting a product base to providing a variety of nonprescription services for patients [45], and new pharmacist services must continue to expand to reflect new social demands as well as historical changes. As trusted health care providers in the community, pharmacists must provide scientific messages in an easy-to-understand manner and contribute to the education and consultation of community residents regarding infectious diseases. A national survey in Japan reported that community residents consulted community pharmacies more about COVID-19 than medicines [3]. A cross-sectional study among Italian community pharmacy clients confirmed that overall satisfaction with pharmacies is high and that the role of community pharmacies is highly valued [47]. In many countries, community pharmacies are the first point of contact with the health care system for people with health-related problems or who simply need information or reliable evidence-based advice. This is essential even in a crisis such as the COVID-19 pandemic [48][49][50].
In the present study, the pharmacist practice reported at the highest frequency was regular cleaning and disinfection activities, followed by keeping social distance from staff and customers. Previous studies indicated that pharmacists, as medical professionals, have basic knowledge about COVID-19 infection control [31,32,38]. However, in the present study, the proportion of pharmacists providing home delivery service of medicines was low, even though pharmacist are well informed about the effectiveness of these services in preventing infection. Implementing a home delivery service necessitates additional requirements for the pharmacy, including human resources and distribution expenses. The low proportion of pharmacies offering this service in the pandemic may reflect these difficulties in implementation. Telemedicine is an effective means of offering consultations, especially during the conditions of infectious disease outbreaks. However, telemedicine may also be limited by institutional conditions as well as national infrastructure conditions. Among the studies that reported the adoption of telemedicine, high proportions of implementation were observed only by studies in the United States and Spain [15,16], with few in low-and middle-income countries [10,[17][18][19].
The present study has some limitations, including those inherent to the nature of systematic reviews and meta-analyses. First, most of the papers included   23:72 in this study were cross-sectional studies and did not necessarily have a high level of evidence. Because the reported outcomes varied among the studies, the number of studies focusing on each practice varied in this meta-analysis. Second, for the purposes of this analysis it was necessary to clearly organize the activities and focus the wide range of pharmacists' community activities on the main action items. The categories of community practice activities for COVID-19 were therefore limited to only the items shown in the target criteria, we selected all reported outcome variables from the extracted papers and selected outcomes variables for the present study. Unreported pharmacy practices may exist in each study due to the survey's focus on defined outcome variables. Third, the published articles included in the study were from only a few countries and did not broadly report practices in many countries. In addition, because the individual observational studies were conducted at different times of the year, we were unable to observe differences in pharmacy practice activities by infection status. Despite these restrictions, the present study is a meta-analysis of pharmacists' practical activities related to COVID-19, showing the potential of pharmacists and providing important insights for expanding the role of pharmacists in the future. Some countries have allowed pharmacists to expand their duties to include practices outside the scope of this study, such as COVID-19 vaccination and prescribing oral therapeutics [51][52][53]. However, this is not the case everywhere. We therefore focused on COVID-19-related activities that can be carried out regardless of national systems and backgrounds, and particularly provision of education and consultation by pharmacists. In addition to being involved in regular medication guidance, this work takes advantage of